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1. Drivers of Speciation Using Genomic Analyses of Two Desert Brittlebush Species, Encelia farinosa and Encelia californica

   Baty, S ; Singhal, S ; Araya-Donoso, R ; Fehlberg, S ; Munguia-Vega, A ; Wilder, B ; Kusumi, K ; Dolby, G ( December 2021 , American Geophysical Union)

   Reproductive isolation is necessary for population divergence to lead to the formation of separate species. This can occur due to physical isolation of populations, which drives allopatric speciation, or other methods of isolation, such as sympatric speciation where the diverging species are physically in the same range, but structural genomic changes or mutations cause the population to diverge into two different species. Parapatric speciation occurs when populations that are geographically adjacent to each other diverge, which can be driven by adaptations to environmental differences, even with ongoing gene flow. Two desert- adapted brittlebush species, Encelia farinosa and Encelia californica, diverged less than 1 million years ago (Singhal et al., 2020) and have a parapatric distribution, residing in different environments in the Mojave and Sonoran deserts. Encelia farinosa (Brittlebush) has unique silvery leaves that are covered in tiny hairs (leaf pubescence) to better control leaf temperature in the hot and arid conditions of the Sonoran Desert. Encelia californica (California Brittlebush) does not display leaf pubescence and is found in a smaller region of the Mediterranean-like environment of the west coast of North America. Encelia californica is exposed to more precipitation than most other Encelia species. Even with their different morphologies, thesemore »two species are still able to hybridize and create fertile offspring (Clark, 1998). Using PacBio sequencing and Hi-C scaffolding, we assembled and annotated reference genomes for both species to investigate the genomic basis of reproductive isolation in these two species. The scaffold N50/L50 are 10 scaffolds and 76.3 Mbp, and 12 scaffolds and 64.5 Mbp for E. farinosa and E. californica, respectively. Using comparative genomic analyses such as tests for differential adaptation and chromosomal translocations will help reveal whether the drivers of speciation in the Encelia radiation were external (e.g., geologic/climatic) or internal (e.g., genomic rearrangement). These analyses will also help answer how accumulated genomic differences can cause speciation in populations that are not geographically isolated. Analyses such as these are new, exciting sources of information for testing geogenomic and other Earth- life hypotheses.« less
2. Geographic and Ecological Dimensions of Host Plant-Associated Genetic Differentiation and Speciation in the Rhagoletis cingulata (Diptera: Tephritidae) Sibling Species Group

   https://doi.org/10.3390/insects10090275  

   Doellman, M ; Schuler, H ; Saintjean, G. ; Hood, G. ; Egan, S. ; Powell, T. ; Glover, M ; Bruzzese, D. ; Smith, J. ; Yee, W. ; et al ( August 2019 , Insects)

   Ascertaining the causes of adaptive radiation is central to understanding how new species arise and come to vary with their resources. The ecological theory posits adaptive radiation via divergent natural selection associated with novel resource use; an alternative suggests character displacement following speciation in allopatry and then secondary contact of reproductively isolated but ecologically similar species. Discriminating between hypotheses, therefore, requires the establishment of a key role for ecological diversification in initiating speciation versus a secondary role in facilitating co-existence. Here, we characterize patterns of genetic variation and postzygotic reproductive isolation for tephritid fruit flies in the Rhagoletis cingulata sibling species group to assess the significance of ecology, geography, and non-adaptive processes for their divergence. Our results support the ecological theory: no evidence for intrinsic postzygotic reproductive isolation was found between two populations of allopatric species, while nuclear-encoded microsatellites implied strong ecologically based reproductive isolation among sympatric species infesting different host plants. Analysis of mitochondrial DNA suggested, however, that cytoplasmic-related reproductive isolation may also exist between two geographically isolated populations within R cingulata. Thus, ecology associated with sympatric host shifts and cytoplasmic effects possibly associated with an endosymbiont may be the key initial drivers of the radiation of the R.more »cingulata group.« less
3. Ancient and recent introgression shape the evolutionary history of pollinator adaptation and speciation in a model monkeyflower radiation (Mimulus section Erythranthe)

   https://doi.org/10.1371/journal.pgen.1009095  

   Nelson, Thomas C. ; Stathos, Angela M. ; Vanderpool, Daniel D. ; Finseth, Findley R. ; Yuan, Yao-wu ; Fishman, Lila ( February 2021 , PLOS Genetics)

   Buerkle, Alex (Ed.)

   Inferences about past processes of adaptation and speciation require a gene-scale and genome-wide understanding of the evolutionary history of diverging taxa. In this study, we use genome-wide capture of nuclear gene sequences, plus skimming of organellar sequences, to investigate the phylogenomics of monkeyflowers in Mimulus section Erythranthe (27 accessions from seven species ) . Taxa within Erythranthe , particularly the parapatric and putatively sister species M . lewisii (bee-pollinated) and M . cardinalis (hummingbird-pollinated), have been a model system for investigating the ecological genetics of speciation and adaptation for over five decades. Across >8000 nuclear loci, multiple methods resolve a predominant species tree in which M . cardinalis groups with other hummingbird-pollinated taxa (37% of gene trees), rather than being sister to M . lewisii (32% of gene trees). We independently corroborate a single evolution of hummingbird pollination syndrome in Erythranthe by demonstrating functional redundancy in genetic complementation tests of floral traits in hybrids; together, these analyses overturn a textbook case of pollination-syndrome convergence. Strong asymmetries in allele sharing (Patterson’s D-statistic and related tests) indicate that gene tree discordance reflects ancient and recent introgression rather than incomplete lineage sorting. Consistent with abundant introgression blurring the history of divergence, low-recombination andmore »adaptation-associated regions support the new species tree, while high-recombination regions generate phylogenetic evidence for sister status for M . lewisii and M . cardinalis . Population-level sampling of core taxa also revealed two instances of chloroplast capture, with Sierran M . lewisii and Southern Californian M . parishii each carrying organelle genomes nested within respective sympatric M . cardinalis clades. A recent organellar transfer from M . cardinalis , an outcrosser where selfish cytonuclear dynamics are more likely, may account for the unexpected cytoplasmic male sterility effects of selfer M . parishii organelles in hybrids with M . lewisii . Overall, our phylogenomic results reveal extensive reticulation throughout the evolutionary history of a classic monkeyflower radiation, suggesting that natural selection (re-)assembles and maintains species-diagnostic traits and barriers in the face of gene flow. Our findings further underline the challenges, even in reproductively isolated species, in distinguishing re-use of adaptive alleles from true convergence and emphasize the value of a phylogenomic framework for reconstructing the evolutionary genetics of adaptation and speciation.« less
4. Hybrid zone or hybrid lineage: a genomic reevaluation of Sibley’s classic species conundrum in Pipilo towhees

   https://doi.org/10.1093/evolut/qpac068  

   DeRaad, Devon A. ; Applewhite, Emily E. ; Tsai, Whitney L. E. ; Terrill, Ryan S. ; Kingston, Sarah E. ; Braun, Michael J. ; McCormack, John E. ( December 2022 , Evolution)

   Hybrid zones can be studied by modeling clines of trait variation (e.g., morphology, genetics) over a linear transect. Yet, hybrid zones can also be spatially complex, can shift over time, and can even lead to the formation of hybrid lineages with the right combination of dispersal and vicariance. We reassessed Sibley’s (1950) gradient between Collared Towhee (Pipilo ocai) and Spotted Towhee (Pipilo maculatus) in Central Mexico to test whether it conformed to a typical tension-zone cline model. By comparing historical and modern data, we found that cline centers for genetic and phenotypic traits have not shifted over the course of 70 years. This equilibrium suggests that secondary contact between these species, which originally diverged over 2 million years ago, likely dates to the Pleistocene. Given the amount of mtDNA divergence, parental ends of the cline have very low autosomal nuclear differentiation (FST = 0.12). Dramatic and coincident cline shifts in mtDNA and throat color suggest the possibility of sexual selection as a factor in differential introgression, while a contrasting cline shift in green back color hints at a role for natural selection. Supporting the idea of a continuum between clinal variation and hybrid lineage formation, the towhee gradient canmore »be analyzed as one population under isolation-by-distance, as a two-population cline, and as three lineages experiencing divergence with gene flow. In the middle of the gradient, a hybrid lineage has become partly isolated, likely due to forested habitat shrinking and fragmenting as it moved upslope after the last glacial maximum and a stark environmental transition. This towhee system offers a window into the potential outcomes of hybridization across a dynamic landscape including the creation of novel genomic and phenotypic combinations and incipient hybrid lineages.

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5. Varied female and male courtship behavior facilitated the evolution of a novel sexual signal

   https://doi.org/10.1093/beheco/arac049  

   Fitzgerald, Sophia L ; Anner, Sophia C ; Tinghitella, Robin M ( June 2022 , Behavioral Ecology)

   Jennions, Michael D (Ed.)

   Abstract Sexual selection can contribute to speciation when signals and preferences expressed during mate choice are coupled within groups, but come to differ across groups (generating assortative mating). When new sexual signals evolve, it is important to investigate their roles in both mate location and courtship contexts, as both signaling functions are critical in mate choice. In previous work, researchers identified two new male morphs (silent and purring) in Hawaiian populations of the Pacific field cricket, Teleogryllus oceanicus. These morphs likely evolved because they protect males from an acoustically orienting parasitoid, yet still obtain some reproductive success. But, it remains unknown how the purring morph functions in close courtship encounters. We compared the relative success of the very recently evolved purring morph to that of the ancestral and silent morphs during courtship encounters. Purring males produce a novel courtship song and were not as successful in courtship as the ancestral type, but were mounted by females as often and as quickly as the obligately silent morph that arose and spread ~20 years ago. Purring males initiate courtship more quickly than other morphs, and females from populations where purring is common exhibit higher overall mounting rates. Thus, differences in the behaviormore »of purring males and of females from populations where purring is common may have facilitated the origin of this novel sexual signal. We found no assortative mating between males of a given morph and females from their own population, and so we hypothesize that multiple male types will be maintained within the species because each achieves fitness in different ways.« less